Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T08:23:48.573Z Has data issue: false hasContentIssue false
  • English
  • Français

New insights into the coexistence of Contracaecum rudolphii A and Contracaecum rudolphii B (Nematoda: Anisakidae) in Phalacrocorax carbo sinensis from Sardinia: genetic variability and phylogenetic analysis

Published online by Cambridge University Press:  03 August 2020

Nabil Amor Open the ORCID record for Nabil Amor [Opens in a new window] ,
Sarra Farjallah ,
Maria Cristina Piras ,
Caterina Burreddu ,
Giovanni Garippa  and
Paolo Merella
Nabil Amor*
Affiliation:
Department of Zoology, KSU Mammals Research Chair, King Saud University, Riyadh11451, Saudi Arabia Laboratory of Biodiversity, Parasitology & Aquatic Ecosystems (LR18ES05) Tunis El Manar University, Tunis2092, Tunisia
Sarra Farjallah
Affiliation:
Laboratory of Biodiversity, Parasitology & Aquatic Ecosystems (LR18ES05) Tunis El Manar University, Tunis2092, Tunisia
Maria Cristina Piras
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, Via Vienna 2, Sassari07100, Italy
Caterina Burreddu
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, Via Vienna 2, Sassari07100, Italy
Giovanni Garippa
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, Via Vienna 2, Sassari07100, Italy
Paolo Merella
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, Via Vienna 2, Sassari07100, Italy
*
Author for correspondence: Nabil Amor, E-mail: [email protected]; [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Contracaecum sp. nematodes are important parasites of fish eating birds that can cause animal health problems. In the present study, specimens of Contracaecum rudolphii sensu lato, from the great cormorant Phalacrocorax carbo sinensis from Sardinia, were characterized based on morphological and molecular data. The morphological analysis allowed to identify all the fourth stage larvae (n = 1918) as Contracaecum sp., and adults, male (n = 5845) and female (n = 8312), as C. rudolphii sensu lato. Population genetics and phylogenetic relationships were inferred based on mitochondrial and nuclear markers. Multiple sequence alignment of the ribosomal internal transcribed spacer showed the coexistence of C. rudolphii A (n = 157), C. rudolphii B (n = 22) and a rare heterozygote of these species. Moreover, mitochondrial markers, namely NADH dehydrogenase subunits I (nad1), cytochrome c oxidase subunit (cox1 and cox2) and small subunit of rRNA (rrnS), showed that the studied C. rudolphii A populations had undergone bottleneck, or founder effect event, subsequent to a rapid population growth and expansion. The observed heterozygote is with a mitochondrial pattern of C. rudolphii B. Although, both Contracaecum species showed high genetic diversity, no genetic structure between localities was detected. Phylogenetic reconstructions supported the paraphyly of the avian Contracaecum species including C. ogmorhini (parasite of otariids).

Keywords

AnisakidaeContracaecum rudolphiiMediterranean SeaPhalacrocorax carbophylogenypopulation genetics
Type
Research Article
Information
Parasitology , Volume 147 , Issue 13 , November 2020 , pp. 1538 - 1551
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abollo, E, Gestal, C and Pascual, S (2001) Anisakid infection in the European shag Phalacrocorax aristotelis aristotelis. Journal of Helminthology 75, 209–214.Google ScholarPubMed
Abollo, E, Paggi, L, Pascual, S and D'Amelio, S (2003) Occurrence of recombinant species of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infection, Genetics and Evolution 3, 175–181.CrossRefGoogle Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Bandelt, HJ, Forster, P and Rohl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Barson, M and Marshall, BE (2004) First record of Contracaecum Spp. (Nematoda:Anisakidae) in fish-eating birds from Zimbabwe. Journal of the South African Veterinary Association 75, 74–78.CrossRefGoogle ScholarPubMed
Barus, V, Sergeeva, TP, Sonin, MD and Ryzhikov, KM (1978) Helminths of Fish-Eating Birds of the Palaearctic Region. I. Nematoda. Prague: Academia. 318p.CrossRefGoogle Scholar
Berland, B (1964) Phocascaris cystophorae sp. nov. (Nematoda) from the hooded seal, with an emendation of the genus. Arbok for Universitetet i Bergen Series Matematica Rerumque Naturalium 17, 1–21.Google Scholar
Bullini, L, Nascetti, G, Paggi, L, Orecchia, P, Mattiucci, S and Berland, B (1986) Genetic variation of ascarid worms with different life cycle. Evolution 40, 437–440.CrossRefGoogle Scholar
Carpegna, F, Grieco, F, Grussu, M, Veronesi, E and Volponi, S (1997) The Italian breeding population of cormorant (Phalacrocorax carbo). Supplementi di Ricerche Biologia Selvaggina XXVI, 81–87.Google Scholar
Cavallero, S, Ligas, A, Bruschi, F and D'Amelio, S (2012) Molecular identification of Anisakis Spp. from fishes collected in the Tyrrhenian Sea (NW Mediterranean). Veterinary Parasitology 187, 563–566.CrossRefGoogle Scholar
Cavallero, S, Costa, A, Caracappa, S, Gambetta, B and D'Amelio, S (2014) Putative hybrids between two Anisakis cryptic species: molecular genotyping using high resolution melting. Experimental Parasitology 146, 87–93.CrossRefGoogle ScholarPubMed
Chang, CT, Tsai, CN, Tang, CY, Chen, CH, Lian, JH, Hu, CY, Tsai, CL, Chao, A, Lai, CH, Wang, TH and Lee, YS (2012) Mixed sequence reader: a program for analyzing DNA sequences with heterozygous base calling. The Scientific World Journal 2012, 10. doi: 10.1100/2012/365104CrossRefGoogle ScholarPubMed
Cole, R and Viney, M (2018) The population genetics of parasitic nematodes of wild animals. Parasites and Vectors 12, 498. doi: https://doi.org/10.1186/s13071-018-3137-5Google Scholar
Culurgioni, J, Sabatini, A, De Murtas, R, Mattiucci, S and Figus, V (2014) Helminth parasites of fish and shellfish from the Santa Gilla Lagoon in southern Sardinia, Italy. Journal of Helminthology 88, 489–498.CrossRefGoogle ScholarPubMed
Dabert, M, Coulson, SJ, Gwiazdowicz, DJ, Moe, B, Hanssen, SA, Biersma, EM, Pilskog, HE and Dabert, J (2015) Differences in speciation progress in feather mites (Analgoidea) inhabiting the same host: the case of Zachvatkinia and Alloptes living on arctic and long-tailed skuas. Experimental and Applied Acarology 65, 163–179.CrossRefGoogle ScholarPubMed
D'Amelio, S, Nascetti, G, Mattiucci, S, Cianchi, R, Orecchia, P, Paggi, L, Berland, B and Bullini, L (1990) Ricerche electroforetiche su alcune specie del genere Contracaecum, parassiti di uccelli ittiofagi (Ascaridida: Anisakidae). Parassitologia 32(suppl. 1), 77.Google Scholar
D'Amelio, S, Barros, NB, Ingrosso, S, Fauquier, DA, Russo, R and Paggi, L (2007) Genetic characterization of members of the genus Contracaecum (Nematoda: Anisakidae) from fish-eating birds from west-central Florida, USA, with evidence of new species. Parasitology 134, 1041–1051.CrossRefGoogle ScholarPubMed
D'Amelio, S, Cavallero, S, Dronen, NO, Barros, NB and Paggi, L (2012) Two new species of Contracaecum Railliet y Henry, 1912 (Nematoda:Anisakidae), C. fagerholmi N. sp. and C. rudolphii F from the brown pelican Pelecanus occidentalis in the northern Gulf of Mexico. Systematic Parasitology 81, 1–16.CrossRefGoogle Scholar
De Jong, MA, Wahlberg, N, van Eijk, M, Brakefield, PM and Zwaan, BJ (2011) Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent refugia. PLoS ONE 6, e21385.CrossRefGoogle ScholarPubMed
Delgado, C and García, G (2015) Coevolution between Contracaecum (Nematoda, Anisakidae) and Austrolebias (Cyprinodontiformes, Rivulidae) host-parasite complex from SW Atlantic coastal basins. Parasitology Research 114, 913–927.CrossRefGoogle ScholarPubMed
Dzido, J, Kijewska, A and Rokicki, J (2012) Selected mitochondrial genes as species markers of the Arctic Contracaecum osculatum complex. Journal of Helminthology 86, 252–258.CrossRefGoogle ScholarPubMed
Excoffier, L and Lischer, HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Fagerholm, HP and Gibson, DI (1987) A redescription of the pinniped parasite Contracaecum ogmorhini (Nematoda, Ascaridoidea), with an assessment of its antiboreal circumpolar distribution. Zoologica Scripta 16, 19–24.CrossRefGoogle Scholar
Farjallah, S, Merella, P, Ingrosso, S, Rotta, A, Slimane, BB, Garippa, G, Said, K and Busi, M (2008a) Molecular evidence for the occurrence of Contracaecum rudolphii A (Nematoda:Anisakidae) in shag Phalacrocorax aristotelis (Linnaeus) (Aves: Phalacrocoracidae) from Sardinia (western Mediterranean Sea). Parasitology International 57, 437–440.CrossRefGoogle Scholar
Farjallah, S, Busi, M, Mahjoub, MO, Slimane, BB, Paggi, L, Said, K and D'Amelio, S (2008b) Molecular characterization of larval anisakid nematodes from marine fishes off the Moroccan and Mauritanian coasts. Parasitology International 57, 430–436.CrossRefGoogle Scholar
Ferreri, M, Qu, W and Han, B (2011) Phylogenetic networks: a tool to display character conflict and demographic history. African Journal of Biotechnology 10, 12799–12803.Google Scholar
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.Google ScholarPubMed
Garbin, L, Mattiucci, S, Paoletti, M, González-Acuña, D and Nascetti, G (2011) Genetic and morphological evidences for the existence of a new species of Contracaecum (Nematoda: Anisakidae) parasite of Phalacrocorax brasilianus (Gmelin) from Chile and its genetic relationships with congeners from fish-eating birds. Journal of Parasitology 97, 476–492.CrossRefGoogle ScholarPubMed
Gasser, RB, Chilton, NB, Hoste, H and Beveridge, I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 2525–2526.CrossRefGoogle ScholarPubMed
Hartwich, G (1964) Revision der vogelparasitischen Nematoden Mitteleuropas II.-Die Gattung Contracaecum Railliet and Henry, 1912 (Ascaridoidea). Mitteilungen aus dem Zoologischen Museum in Berlin 40, 15–53.Google Scholar
Hartwich, G (1974) Keys to genera of the Ascaridoidea. In Anderson, RC, Chabaud, AG and Willmott, S (eds), CIH Keys to the Nematode Parasites of Vertebrates. Farnham Royal England: Commonwealth Agricultural Bureaux, pp. 1–15.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2016) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773. doi: dx.doi.org/10.1093/molbev/msw260Google Scholar
Levin, II and Parker, PG (2013) Comparative host–parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds. Parasitology 140, 1061–1069.CrossRefGoogle ScholarPubMed
Li, A, D'Amelio, S, Paggi, L, He, F, Gasser, RB, Lun, Z, Abollo, E, Turchetto, M and Zhu, X (2005) Genetic evidence for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) and the validity of Contracaecum septentrionale (Kreis, 1955) (Nematoda: Anisakidae). Parasitology Research 96, 361–366.CrossRefGoogle Scholar
Librado, P and Rozas, J (2009) DnaSP v5. A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lin, RQ, Liu, GH, Zhang, Y, D'Amelio, S, Zhou, DH, Yuan, ZG, Zou, FC, Song, HQ and Zhu, XQ (2012) Contracaecum rudolphii B: gene content, arrangement and composition of its complete mitochondrial genome compared with Anisakis simplex s.l. Experimental Parasitology 130, 135–140.CrossRefGoogle ScholarPubMed
Marques, JF, Cabral, HN, Busi, M and D'Amelio, S (2006) Molecular identification of Anisakis species from Pleuronectiformes off the Portuguese coast. Journal of Helminthology 80, 47–51.CrossRefGoogle ScholarPubMed
Mattiucci, S, Cianchi, R, Nascetti, G, Paggi, L, Sardella, N, Timmi, J, Webb, SC, Bastida, R, Rodriquez, D and Bullini, L (2003) Genetic evidence for two sibling species within Contracaecum ogmorhini Johnston & Mawson, 1941 (Nematoda: Anisakidae) from otariid seals of boreal and austral regions. Systematic Parasitology 54, 13–23.CrossRefGoogle ScholarPubMed
Mattiucci, S, Paoletti, M, Webb, SC, Sardella, N, Timi, JT, Berland, B and Nascetti, G (2008) Genetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda: Anisakidae) from pinnipeds inferred from mitochondrial cox2 sequences, and congruence with allozyme data. Parasite 15, 408–419.Google ScholarPubMed
Mattiucci, S, Paoletti, M, Solorzano, AC and Nascetti, G (2010) Contracaecum gibsoni n. sp. and C. overstreeti N. sp. (Nematoda: Anisakidae) from the Dalmatian pelican Pelecanus crispus (L.) in Greek waters: genetic and morphological evidence. Systematic Parasitology 75, 207–224.CrossRefGoogle Scholar
Mattiucci, S, Sbaraglia, GL, Palomba, M, Filippi, S, Paoletti, M, Cipriani, P and Nascetti, G (2020) Genetic identification and insights into the ecology of Contracaecum rudolphii A and C. rudolphii B (Nematoda: Anisakidae) from cormorants and fish of aquatic ecosystems of Central Italy. Parasitology Research 119, 1243–1257. doi: 10.1007/s00436-020-06658-8CrossRefGoogle Scholar
Molnár, K, Székely, C, Baska, F, Müller, T, Zuo, S, Kania, PW, Nowak, B and Buchmann, K (2019) Differential survival of 3rd stage larvae of Contracaecum rudolphii type B infecting common bream (Abramis brama) and common carp (Cyprinus carpio). Parasitol Res 7, 1–7.Google Scholar
Nadler, SA (2000) Hudspeth DSS. Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. Journal of Parasitology 86, 380–394.CrossRefGoogle Scholar
Nadler, SA, D'Amelio, S, Fagerholm, HP, Berland, B and Paggi, L (2000) Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121, 455–463.CrossRefGoogle ScholarPubMed
Nadler, SA, D'Amelio, S, Dailey, MD, Paggi, L, Siu, S and Sakanari, JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. Journal of Parasitology 91, 1413–1429.CrossRefGoogle ScholarPubMed
Okonechnikov, K, Golosova, , Fursov, M and the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28, 1166–1167.CrossRefGoogle ScholarPubMed
Orecchia, P, Mattiucci, S, D'Amelio, S, Paggi, L, Plotz, J, Cianchi, R, Nascetti, G, Arduino, P and Bullini, L (1994) Two new members in the Contracaecum osculatum complex (Nematoda: Ascaridoidea) from the Antarctic. International Journal for Parasitology 24, 367–377.CrossRefGoogle ScholarPubMed
Pichler, FB (2002) Genetic assessment of population boundaries and gene exchange in Hector's dolphin. DOC Science Internal Series 44, 1–36.Google Scholar
Rand, DM, Dorfsman, M and Kann, LM (1994) Neutral and non-neutral evolution of drosophila mitochondrial DNA. Genetics 138, 741–756.Google ScholarPubMed
Schmid, KJ, Nigro, L, Aquadro, CF and Tautz, D (1999) Large number of replacement polymorphisms in rapidly evolving genes of Drosophila: implications for genome-wide surveys of DNA polymorphism. Genetics 153, 1717–1729.Google ScholarPubMed
Shamsi, S (2019) Parasite loss or parasite gain? Story of Contracaecum nematodes in antipodean waters. Parasite Epidemiology and Control 4, e00087. doi: 10.1016/j.parepi.2019.e00087CrossRefGoogle ScholarPubMed
Shamsi, S, Norman, R, Gasser, R and Beveridge, I (2009) Genetic and morphological evidences for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) (Nematoda: Anisakidae) in Australia. Parasitology Research 105, 529–538.CrossRefGoogle ScholarPubMed
Slatkin, M and Hudson, RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.Google ScholarPubMed
Stamatakis, A (2006) Raxml-vi-hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.Google ScholarPubMed
Szostakowska, B and Fagerholm, HP (2007) Molecular identification of two strains of third-stage larvae of Contracaecum rudolphii sensu lato (Nematoda: Anisakidae) from fish in Poland. Journal of Parasitology 93, 961–964.Google ScholarPubMed
Szostakowska, B and Fagerholm, HP (2012) Coexistence and genetic variability of Contracaecum rudolphii A and Contracaecum rudolphii B (Nematoda: Anisakidae) in cormorants, Phalacrocorax carbo sinensis, in the Baltic Region. Journal of Parasitology 98, 472–478.CrossRefGoogle ScholarPubMed
Szostakowska, B, Myjak, P and Kur, J (2002) Identification of anisakid nematodes from the Southern Baltic Sea using PCR-based methods. Molecular and Cellular Probes 16, 111–118.CrossRefGoogle ScholarPubMed
Szudarek, N, Kanarek, G and Dabert, J (2017) The genetic structure of hypoderatid mites (Actinotrichida: Astigmata) parasitizing great cormorant (Phalacrocorax carbo) during host post-breeding dispersal in Milicz, SW Poland. Acta Parasitologica 62, 76–89.CrossRefGoogle ScholarPubMed
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google ScholarPubMed
Supplementary material: File

Amor et al. supplementary material

Tables S1-S3

Download Amor et al. supplementary material(File)
File 31.7 KB